Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities

The ecological effects of ocean acidification (OA) from rising atmospheric carbon dioxide (CO₂) on benthic marine communities are largely unknown. We investigated in situ the consequences of long-term exposure to high CO₂ on coral-reef-associated macroinvertebrate communities around three shallow volcanic CO₂ seeps in Papua New Guinea. The densities of many groups and the number of taxa (classes and phyla) of macroinvertebrates were significantly reduced at elevated CO₂ (425–1100 µatm) compared with control sites. However, sensitivities of some groups, including decapod crustaceans, ascidians and several echinoderms, contrasted with predictions of their physiological CO₂ tolerances derived from laboratory experiments. High CO₂ reduced the availability of structurally complex corals that are essential refugia for many reef-associated macroinvertebrates. This loss of habitat complexity was also associated with losses in many macroinvertebrate groups, especially predation-prone mobile taxa, including crustaceans and crinoids. The transition from living to dead coral as substratum and habitat further altered macroinvertebrate communities, with far more taxa losing than gaining in numbers. Our study shows that indirect ecological effects of OA (reduced habitat complexity) will complement its direct physiological effects and together with the loss of coral cover through climate change will severely affect macroinvertebrate communities in coral reefs.     

Calcification rates and the effect of ocean acidification on Mediterranean cold-water corals

Global environmental changes, including ocean acidification, have been identified as a major threat to scleractinian corals. General predictions are that ocean acidification will be detrimental to reef growth and that 40 to more than 80 per cent of present-day reefs will decline during the next 50 years. Cold-water corals (CWCs) are thought to be strongly affected by changes in ocean acidification owing to their distribution in deep and/or cold waters, which naturally exhibit a CaCO(3) saturation state lower than in shallow/warm waters. Calcification was measured in three species of Mediterranean cold-water scleractinian corals (Lophelia pertusa, Madrepora oculata and Desmophyllum dianthus) on-board research vessels and soon after collection. Incubations were performed in ambient sea water. The species M. oculata was additionally incubated in sea water reduced or enriched in CO(2). At ambient conditions, calcification rates ranged between -0.01 and 0.23% d(-1). Calcification rates of M. oculata under variable partial pressure of CO(2) (pCO(2)) were the same for ambient and elevated pCO(2) (404 and 867 μatm) with 0.06 ± 0.06% d(-1), while calcification was 0.12 ± 0.06% d(-1) when pCO(2) was reduced to its pre-industrial level (285 μatm). This suggests that present-day CWC calcification in the Mediterranean Sea has already drastically declined (by 50%) as a consequence of anthropogenic-induced ocean acidification.     

Effects of ocean acidification on learning in coral reef fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO(2) predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO(2) effects, whereby some individuals are unaffected at particular CO(2) concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 μatm CO(2) (current day levels) or 850 μatm CO(2), a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO(2) failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 μatm-CO(2) fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO(2) exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO(2) exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO(2)-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO(2) may alter the cognitive ability of juvenile fish and render learning ineffective.     

Stress-tolerant corals of Florida Bay are vulnerable to ocean acidification

In situ calcification measurements tested the hypothesis that corals from environments (Florida Bay, USA) that naturally experience large swings in pCO₂ and pH will be tolerant or less sensitive to ocean acidification than species from laboratory experiments with less variable carbonate chemistry. The pCO₂ in Florida Bay varies from summer to winter by several hundred ppm roughly comparable to the increase predicted by the end of the century. Rates of net photosynthesis and calcification of two stress-tolerant coral species, Siderastrea radians and Solenastrea hyades, were measured under the prevailing ambient chemical conditions and under conditions amended to simulate a pH drop of 0.1–0.2 units at bimonthly intervals over a 2-yr period. Net photosynthesis was not changed by the elevation in pCO₂ and drop in pH; however, calcification declined by 52 and 50 % per unit decrease in saturation state, respectively. These results indicate that the calcification rates of S. radians and S. hyades are just as sensitive to a reduction in saturation state as coral species that have been previously studied. In other words, stress tolerance to temperature and salinity extremes as well as regular exposure to large swings in pCO₂ and pH did not make them any less sensitive to ocean acidification. These two species likely survive in Florida Bay in part because they devote proportionately less energy to calcification than most other species and the average saturation state is elevated relative to that of nearby offshore water due to high rates of primary production by seagrasses.     

Independent effects of ocean warming versus acidification on the growth,survivorship and physiology of two Acropora corals

Coral Reefs - Climate change is the greatest threat to coral reef ecosystems. Importantly, gradual changes in seawater chemistry compounds upon increasing temperatures leading to declines in...     

Combined ocean acidification and low temperature stressors cause coral mortality

Oceans are predicted to become more acidic and experience more temperature variability—both hot and cold—as climate changes. Ocean acidification negatively impacts reef-building corals, especially when interacting with other stressors such as elevated temperature. However, the effects of combined acidification and low temperature stress have yet to be assessed. Here, we exposed nubbins of the scleractinian coral Montipora digitata to ecologically relevant acidic, cold, or combined stress for 2 weeks. Coral nubbins exhibited 100% survival in isolated acidic and cold treatments, but ~30% mortality under combined conditions. These results provide further evidence that coupled stressors have an interactive effect on coral physiology, and reveal that corals in colder environments are also susceptible to the deleterious impacts of coupled ocean acidification and thermal stress.     

Hidden impacts of ocean acidification to live and dead coral framework

Cold-water corals, such as Lophelia pertusa, are key habitat-forming organisms found throughout the world''s oceans to 3000 m deep. The complex three-dimensional framework made by these vulnerable marine ecosystems support high biodiversity and commercially important species. Given their importance, a key question is how both the living and the dead framework will fare under projected climate change. Here, we demonstrate that over 12 months L. pertusa can physiologically acclimate to increased CO₂, showing sustained net calcification. However, their new skeletal structure changes and exhibits decreased crystallographic and molecular-scale bonding organization. Although physiological acclimatization was evident, we also demonstrate that there is a negative correlation between increasing CO₂ levels and breaking strength of exposed framework (approx. 20–30% weaker after 12 months), meaning the exposed bases of reefs will be less effective ‘load-bearers’, and will become more susceptible to bioerosion and mechanical damage by 2100.     

Resolving the interactions of ocean acidification and temperature on coral calcification media pH

Coral Reefs - Ocean acidification typically reduces the calcification rates of massive Porites spp. corals, but increasing seawater temperatures (below the stress and bleaching threshold) can...     

Major cellular and physiological impacts of ocean acidification on a reef building coral

As atmospheric levels of CO(2) increase, reef-building corals are under greater stress from both increased sea surface temperatures and declining sea water pH. To date, most studies have focused on either coral bleaching due to warming oceans or declining calcification due to decreasing oceanic carbonate ion concentrations. Here, through the use of physiology measurements and cDNA microarrays, we show that changes in pH and ocean chemistry consistent with two scenarios put forward by the Intergovernmental Panel on Climate Change (IPCC) drive major changes in gene expression, respiration, photosynthesis and symbiosis of the coral, Acropora millepora, before affects on biomineralisation are apparent at the phenotype level. Under high CO(2) conditions corals at the phenotype level lost over half their Symbiodinium populations, and had a decrease in both photosynthesis and respiration. Changes in gene expression were consistent with metabolic suppression, an increase in oxidative stress, apoptosis and symbiont loss. Other expression patterns demonstrate upregulation of membrane transporters, as well as the regulation of genes involved in membrane cytoskeletal interactions and cytoskeletal remodeling. These widespread changes in gene expression emphasize the need to expand future studies of ocean acidification to include a wider spectrum of cellular processes, many of which may occur before impacts on calcification.     

Decline in symbiont densities of tropical and subtropical scleractinian corals under ocean acidification

Coral Reefs - Ocean acidification changes the carbonate chemistry of seawater in a manner that reduces the biomineralisation rate of reef-building corals. Other effects of acidification on coral...     

Differential response of two Mediterranean cold-water coral species to ocean acidification

Cold-water coral (CWC) reefs constitute one of the most complex deep-sea habitats harboring a vast diversity of associated species. Like other tropical or temperate framework builders, these systems are facing an uncertain future due to several threats, such as global warming and ocean acidification. In the case of Mediterranean CWC communities, the effect may be exacerbated due to the greater capacity of these waters to absorb atmospheric CO₂ compared to the global ocean. Calcification in these organisms is an energy-demanding process, and it is expected that energy requirements will be greater as seawater pH and the availability of carbonate ions decrease. Therefore, studies assessing the effect of a pH decrease in skeletal growth, and metabolic balance are critical to fully understand the potential responses of these organisms under a changing scenario. In this context, the present work aims to investigate the medium- to long-term effect of a low pH scenario on calcification and the biochemical composition of two CWCs from the Mediterranean, Dendrophyllia cornigera and Desmophyllum dianthus. After 314 d of exposure to acidified conditions, a significant decrease of 70 % was observed in Desmophyllum dianthus skeletal growth rate, while Dendrophyllia cornigera showed no differences between treatments. Instead, only subtle differences between treatments were observed in the organic matter amount, lipid content, skeletal microdensity, or porosity in both species, although due to the high variability of the results, these differences were not statistically significant. Our results also confirmed a heterogeneous effect of low pH on the skeletal growth rate of the organisms depending on their initial weight, suggesting that those specimens with high calcification rates may be the most susceptible to the negative effects of acidification.     

A corrosive concoction: The combined effects of ocean warming and acidification on the early growth of a stony coral are multiplicative

Survival of coral planulae, and the successful settlement and healthy growth of primary polyps are critical for the dispersal of scleractinian corals and hence the recovery of degraded coral reefs. It is therefore important to explore how the warmer and more acidic oceanic conditions predicted for the future could affect these processes. This study used controlled culture to investigate the effects of a 1 °C increase in temperature and a 0.2-0.25 unit decrease in pH on the settlement and survival of planulae and the growth of primary polyps in the Tropical Eastern Pacific coral Porites panamensis. We found that primary polyp growth was reduced only marginally by more acidic seawater but the combined effect of high temperature and lowered pH caused a significant reduction in growth of primary polyps by almost a third. Elevated temperature was found to significantly reduce the amount of zooxanthellae in primary polyps, and when combined with lowered pH resulted in a significant reduction in biomass of primary polyps. However, survival and settlement of planula larvae were unaffected by increased temperature, lowered acidity or the combination of both. These results indicate that in future scenarios of increased temperature and oceanic acidity coral planulae will be able to disperse and settle successfully but primary polyp growth may be hampered. The recovery of reefs may therefore be impeded by global change even if local stressors are curbed and sufficient sources of planulae are available.     

Responses of a coral reef shark acutely exposed to ocean acidification conditions

Anthropogenic ocean acidification (OA) is a threat to coral reef fishes, but few studies have investigated responses of high-trophic-level predators, including sharks. We tested the effects of 72-hr exposure to OA-relevant elevated partial pressures of carbon dioxide (pCO₂) on oxygen uptake rates, acid–base status, and haematology of newborn tropical blacktip reef sharks (Carcharhinus melanopterus). Acute exposure to end-of-century pCO₂ levels resulted in elevated haematocrit (i.e. stress or compensation of oxygen uptake rates) and blood lactate concentrations (i.e. prolonged recovery) in the newborns. Conversely, whole blood and mean corpuscular haemoglobin concentrations, blood pH, estimates of standard and maximum metabolic rates, and aerobic scope remained unaffected. Taken together, newborn blacktip reef sharks appear physiologically robust to end-of-century pCO₂ levels, but less so than other, previously investigated, tropical carpet sharks. Our results suggest peak fluctuating pCO₂ levels in coral reef lagoons could still physiologically affect newborn reef sharks, but studies assessing the effects of long-term exposure and in combination with other anthropogenic stressors are needed.

     

Intrageneric variation in antipredator responses of coral reef fishes affected by ocean acidification: implications for climate change projections on marine communities

Our planet is experiencing an increase in the concentration of atmospheric carbon dioxide (CO₂) unprecedented in the past 800 000 years. About 30% of excess atmospheric CO₂ is absorbed by the oceans, thus increasing the concentration of carbonic acid and reducing the ocean's pH. Species able to survive the physiological stress imposed by ocean acidification may still suffer strong indirect negative consequences. Comparing the tolerance of different species to dissolved CO₂ is a necessary first step towards predicting the ecological impacts of rising CO₂ levels on marine communities. While it is intuitive that not all aquatic species will be affected the same way by CO₂, one could predict that closely related species, sharing similar life histories and ecology, may show similar tolerance levels to CO₂. Our ability to create functional groups of species according to their CO₂ tolerance may be crucial in our ability to predict community change in the future. Here, we tested the effects of CO₂ exposure on the antipredator responses of four damselfish species (Pomacentrus chrysurus, Pomacentrus moluccensis, Pomacentrus amboinensis and Pomacentrus nagasakiensis). Although being sympatric and sharing the same ecology and life history, the four congeneric species showed striking and unexpected variation in CO₂ tolerance, with CO₂‐induced loss of response to predation risk ranging from 30% to 95%. Using P. chrysurus as a model species, we further tested if these behavioural differences translated into differential ability to survive predators under natural conditions. Our results indicate that P. chrysurus larvae raised under CO₂ levels predicted by 2070 and 2100 showed decreased antipredator responses to risk, leading to a five‐ to sevenfold increase in predation‐related mortality in the first few hours of settlement. Examining ocean acidification, along with other environmental variables, will be a critical step in further evaluating ecological responses to predicted climatic change.     

Calcifying coral abundance near low-pH springs: implications for future ocean acidification

Rising atmospheric CO₂ and its equilibration with surface ocean seawater is lowering both the pH and carbonate saturation state (Ω) of the oceans. Numerous calcifying organisms, including reef-building corals, may be severely impacted by declining aragonite and calcite saturation, but the fate of coral reef ecosystems in response to ocean acidification remains largely unexplored. Naturally low saturation (Ω ~ 0.5) low pH (6.70–7.30) groundwater has been discharging for millennia at localized submarine springs (called “ojos”) at Puerto Morelos, México near the Mesoamerican Reef. This ecosystem provides insights into potential long term responses of coral ecosystems to low saturation conditions. In-situ chemical and biological data indicate that both coral species richness and coral colony size decline with increasing proximity to low-saturation, low-pH waters at the ojo centers. Only three scleractinian coral species (Porites astreoides, Porites divaricata, and Siderastrea radians) occur in undersaturated waters at all ojos examined. Because these three species are rarely major contributors to Caribbean reef framework, these data may indicate that today’s more complex frame-building species may be replaced by smaller, possibly patchy, colonies of only a few species along the Mesoamerican Barrier Reef. The growth of these scleractinian coral species at undersaturated conditions illustrates that the response to ocean acidification is likely to vary across species and environments; thus, our data emphasize the need to better understand the mechanisms of calcification to more accurately predict future impacts of ocean acidification.     

Impacts of ocean acidification and burrowing urchins on within-sediment pH profiles and subtidal nematode communities

Rising carbon dioxide levels in the atmosphere will affect the ocean carbonate system, resulting in a predicted future decrease in the pH of seawater by 0.3-0.5 units. To investigate whether the presence of a burrowing urchin, Echinocardium cordatum, might influence the impact of ocean acidification on subtidal sediment pH profiles and nematode community structure an experiment was conducted using subtidal sediment, with urchins present or absent and seawater at either pH 8.0 (ambient) or 7.5. The presence of urchins, and a reduction in pH, both had significant effects on within-sediment pH profiles. Where urchins were present sediment profiles were more consistent and sediment pH was lower than that of the overlying seawater. There were significant differences in nematode abundance between treatments. The primary effect was a higher abundance of nematodes in replicates with urchins in natural seawater. All treatments had similar nematode community structure and diversity. Ocean acidification could therefore lead to changes in nematode communities in subtidal sediments affected by burrowing urchins.     

Molecular mechanisms underlying the physiological responses of the cold-water coral Desmophyllum dianthus to ocean acidification

Cold-water corals (CWCs) are thought to be particularly vulnerable to ocean acidification (OA) due to increased atmospheric pCO₂, because they inhabit deep and cold waters where the aragonite saturation state is naturally low. Several recent studies have evaluated the impact of OA on organism-level physiological processes such as calcification and respiration. However, no studies to date have looked at the impact at the molecular level of gene expression. Here, we report results of a long-term, 8-month experiment to compare the physiological responses of the CWC Desmophyllum dianthus to OA at both the organismal and gene expression levels under two pCO₂/pH treatments: ambient pCO₂ (460 μatm, pH_T = 8.01) and elevated pCO₂ (997 μatm, pH_T = 7.70). At the organismal level, no significant differences were detected in the calcification and respiration rates of D. dianthus. Conversely, significant differences were recorded in gene expression profiles, which showed an up-regulation of genes involved in cellular stress (HSP70) and immune defence (mannose-binding c-type lectin). Expression of alpha-carbonic anhydrase, a key enzyme involved in the synthesis of coral skeleton, was also significantly up-regulated in corals under elevated pCO₂, indicating that D. dianthus was under physiological reconditioning to calcify under these conditions. Thus, gene expression profiles revealed physiological impacts that were not evident at the organismal level. Consequently, understanding the molecular mechanisms behind the physiological processes involved in a coral’s response to elevated pCO₂ is critical to assess the ability of CWCs to acclimate or adapt to future OA conditions.